Summary People find it easier to learn about topics that interest them, but little is known about the mechanisms by which intrinsic motivational states affect learning. We used functional magnetic resonance imaging to investigate how curiosity (intrinsic motivation to learn) influences memory. In both immediate and one-day delayed memory tests, participants showed improved memory for information that they were curious about, and also for incidental material learned during states of high curiosity. FMRI results revealed that activity in the midbrain and the nucleus accumbens was enhanced during states of high curiosity. Importantly, individual variability in curiosity-driven memory benefits for incidental material was supported by anticipatory activity in the midbrain and hippocampus and by functional connectivity between these regions. These findings suggest a link between the mechanisms supporting extrinsic reward motivation and intrinsic curiosity and highlight the importance of stimulating curiosity in order to create more effective learning experiences.

SUMMARY The hippocampus is critical for human episodic memory, but its role remains controversial. One fundamental question concerns whether the hippocampus represents specific objects or assigns context-dependent representations to objects. Here, we used multivoxel pattern similarity analysis of fMRI data during retrieval of learned object sequences to systematically investigate hippocampal coding of object and temporal context information. Hippocampal activity patterns carried information about the temporal positions of objects in learned sequences, but not about objects or temporal positions in random sequences. Hippocampal activity patterns differentiated between overlapping object sequences and between temporally adjacent objects that belonged to distinct sequence contexts. Parahippocampal and perirhinal cortex showed different pattern information profiles consistent with coding of temporal position and object information, respectively. These findings are consistent with models proposing that the hippocampus represents objects within specific temporal contexts, a capability that might explain its critical role in episodic memory.

Reward motivation is known to modulate memory encoding, and this effect depends on interactions between the substantia nigra/ ventral tegmental area complex (SN/VTA) and the hippocampus. It is unknown, however, whether these interactions influence offline neural activity in the human brain that is thought to promote memory consolidation. Here, we used functional magnetic resonance imaging (fMRI) to test the effect of reward motivation on post-learning neural dynamics and subsequent memory for objects that were learned in high- or low-reward motivation contexts. We found that post-learning increases in resting-state functional connectivity between the SN/VTA and hippocampus predicted preferential retention of objects that were learned in high-reward contexts. In addition, multivariate pattern classification revealed that hippocampal representations of high-reward contexts were preferentially reactivated during post-learning rest, and the number of hippocampal reactivations was predictive of preferential retention of items learned in high-reward contexts. These findings indicate that reward motivation alters offline post-learning dynamics between the SN/VTA and hippocampus, providing novel evidence for a potential mechanism by which reward could influence memory consolidation.

Curiosity plays a fundamental role for learning and memory, but the neural mechanisms that stimulate curiosity and its effect on memory are poorly understood. Accumulating evidence suggests that curiosity states are related to modulations in activity in the dopaminergic circuit and that these modulations impact memory encoding and consolidation for both targets of curiosity and incidental information encountered during curiosity states. To account for this evidence, we propose the Prediction, Appraisal, Curiosity, and Exploration (PACE) framework, which attempts to explain curiosity and memory in terms of cognitive processes, neural circuits, behavior, and subjective experience. The PACE framework generates testable predictions that can stimulate future investigation of the mechanisms underlying curiosity-related memory enhancements.

A new development in our understanding of human long-term memory is that effective memory formation relies on neural activity just before an event. It is unknown whether such prestimulus activity is under voluntary control or a reflection of random fluctuations over time. In the present study, we addressed two issues: (1) whether prestimulus activity is influenced by an individual's motivation to encode, and (2) at what point in time encoding-related activity emerges. Electrical brain activity was recorded while healthy male and female adults memorized series of words. Each word was preceded by a cue, which indicated the monetary reward that would be received if the following word was later remembered. Memory was tested after a short delay with a five-way recognition task to separate different sources of recognition. Electrical activity elicited by the reward cue predicted later memory of a word. Crucially, however, this was only observed when the incentive to memorize a word was high. Encoding-related activity preceded high-reward words that were later recollected. This activity started shortly after cue onset and persisted until word onset. Prestimulus activity thus not only signals cue-related processing but also an ensuing preparatory state. In contrast, reward-related activity was limited to the time period immediately after the reward cue. These findings indicate that engaging neural activity that benefits the encoding of an upcoming event is under voluntary control, reflecting a strategic preparatory state in anticipation of processing an event.